research article soil microbial community structure...

Research ArticleSoil Microbial Community Structure Evolution along HalophyteSuccession in Bohai Bay Wetland

Mingyang Cong1 Di Cao2 Jingkuan Sun3 and Fuchen Shi1

1 Department of Plant Biology amp Ecology College of Life Sciences Nankai University Weijin Road 94 Tianjin 300071 China2 College of Life Science and Technology Heilongjiang Bayi Agricultural University Daqing 163319 China3 Research Center for Eco-Environmental Sciences of Yellow River Delta Binzhou University Binzhou 256600 China

Correspondence should be addressed to Fuchen Shi fcshinankaieducn

Received 27 June 2014 Revised 4 October 2014 Accepted 18 October 2014 Published 9 November 2014

Academic Editor Huiwang Gao

Copyright copy 2014 Mingyang Cong et alThis is an open access article distributed under theCreativeCommonsAttribution Licensewhich permits unrestricted use distribution and reproduction in any medium provided the original work is properly cited

It is urgent to recover Bohai Bay costal wetland ecosystem because of covering a large area of severe saline-alkali soil To explorethe relationship between halophyte herbaceous succession and microbial community structure we chose four local communitieswhich played an important role in improving soil microenvironmentWe performed phospholipid fatty acid analysis measured soilparameters and evaluated shifts of microbial community structure Results showed that microbial community structure changedsignificantly along succession and bacteria community was dominant Total phospholipid fatty acid content increased in differentsuccessional stages but decreased with depth with similar variations in bacterial and fungal biomass Soil organic carbon andespecially total nitrogen were positively correlated with microbial biomass Colonization of pioneering salt-tolerant plants Suaedaglauca in saline-alkali bare land changed total soilmicroorganism content and compositionThese results showed that belowgroundprocesses were strongly related with aboveground halophyte succession Fungalbacterial ratio Gram-negativeGram-positivebacteria ratio total microbial biomass and fungi and bacteria content could indicate the degree of succession stages in BohaiBay wetland ecosystem And also these findings demonstrated that microbial community biomass and composition evolved alongwith vegetation succession environmental variables

1 Introduction

Vegetation soil and microbes depend on and restrict eachother [1] Microbes are sensitive to external environmentalchanges and the most remarkable characteristic is the abilityto change the community structure [2] The role of soilmicroorganisms in the ecosystem is to decompose organicmatter in the soil and promote formation of humus [3 4]absorb fix and release nutrients and improve and regulatenutrition in plants [5 6] Previous studies examining relation-ship between vegetation succession andmicrobial communi-ties were conducted in a forest ecosystem [7] karst ecosystem[8] or volcanic desert ecosystem [9] However studieson examining an extreme saline-alkali wetland ecosystemare rare Beidagang wetland is one of the most importantwetlands located in Bohai Bay which is officially includedin ldquolist of important wetlands in Chinardquo Coastal wetlandsare fragile and sensitive ecological areas with poor soil On

account of different climate and soil conditions from inlandthe vegetation has unique characteristics High salinity soilsamples from four plots representing different successionalstages were collected for this study Main local halophyte instudy site included Suaeda glauca and Phragmites australisSuaeda glauca is a kind of leafy succulent plant that canaccumulate salt ions Such a strong alkali euhalophyte candecrease the salt content of topsoil during growing seasonOnthe contrary Phragmites australis is a kind of salt-excludingplant which can reduce its own salt concentration throughphysiological structure of cell membrane in roots [10]

A phospholipid fatty acid (PLFA) method was employedto examine the soil microbial community PLFAs are impor-tant components of living microbe cell membrane and aresynthesized by various microorganisms through differentbiochemical pathways Thus PLFAs can accurately expressthe biomass and composition of the soil microbial commu-nity [11]

Hindawi Publishing CorporationJournal of ChemistryVolume 2014 Article ID 491347 8 pageshttpdxdoiorg1011552014491347

2 Journal of Chemistry

Tianjin

0 125 25(km)

SS

Bohai Bay

Beidag

ang

SS

Beidagang ReservoirBL

SGSG+PA

PA

Bohai Bay

N

W E

S

117∘09

9984000998400998400E 117

∘21

9984000998400998400E 117

∘33

9984000998400998400E 117

∘45

9984000998400998400E 117

∘57

9984000998400998400E

39∘03

9984000998400998400N

37∘57

9984000998400998400N

38∘51

9984000998400998400N

38∘45

9984000998400998400N

38∘39

9984000998400998400N

Figure 1 Locations of study and sample sites (SS) near the Bohai Bay Details of the plots and abbreviation names of dominant species arelisted in Table 1

The aims of this study were to elucidate (1) the response ofmicroorganism community structural composition to alongwith environmental changes caused by halophyte successionand (2) main factors influencing soil microbial commu-nity structure along with succession The results of thisstudy may offer critical information for ecological restora-tion and soil quality improvement in severe saline-alkaliwetlands

2 Materials and Methods

21 Study Sites It was located in the southeast of Tianjin nearBohai Bay middle-east of China (117∘271015840E 38∘431015840N) (Figure 1and Table 1) It was characterized by a warm semihumidcontinental monsoon climate Annual mean temperaturewas approximately 122∘C with the coldest (January) andhottest (July) mean temperatures of 35∘C and 262∘C respec-tively Annual mean precipitation was 520ndash660mm and 75was summer rainfall (JulyndashSeptember) The study area wascovered by extreme saline-alkali soil together with larger

amount of evaporation and smaller amount of precipitationThe soil in this area was barren Landform was a coastalfloodplain with sparse vegetation

22 Soil Sampling We investigated four community typeswith three repetitions in June 2013 Table 1 summarized theinformation of four successional stages covering averageheight coverage biomass and altitude of dominant speciesThe four typical communities examined were (I) saline-alkalibare land (BL) (II) Suaeda glauca community (SG) (III)Suaeda glauca + Phragmites australis community (SG + PA)and (IV) Phragmites australis community (PA) Soil sampleswere collected using multipoint mixed method with threevertical layers S1 (0ndash10 cm) S2 (10ndash20 cm) and S3 (20ndash30 cm) We collected in two times on account of differentanalyses One set was used to measure bulk density andmoisture content by a cutting ring Another set was dividedinto twoparts for PLFAanalysis kept atminus20∘C for parameteranalyses dried in shade homogenized and sieved beforepreserved

Journal of Chemistry 3

Table 1 Dominant species in plots

Stage Plant community Average height (cm) Coverage () Biomass (gmminus2) Altitude (m)I Saline-alkali bare land mdash mdash mdash 10II Suaeda glauca 16 74 18 plusmn 04 103

III Suaeda glauca + Phragmites australis 24 69 23 plusmn 03 106109 66 169 plusmn 10 106

IV Phragmites australis 136 83 192 plusmn 7 11

23 Soil Physicochemical Analyses Soil organic carbon(SOC) and total nitrogen (TN) were measured by combus-tion using a macroelement analyzer (vario MACRO CNElementar Analysensysteme GmbH Germany) Bulk densityand moisture content were determined with samples driedin oven at 105∘C for 48 h until a constant weight Soil pHwas determined with air-dried soil (soil water 1 25) usinga glass electrode Sartorius PB-10 pH meter (Sartorius Ger-many) Salinity was determined by drying-weighing methodFiltrate (soil water 1 5) was placed in oven at 105∘C toconstant weight

24 Phospholipid Fatty Acid Analysis (PLFA) PLFAs arefound in living microbial cell membranes and can be used asmarkers of biomass and a fingerprint of the microorganismcommunity structure [2 12] PLFAaffords a quick and reliablemethod for estimating microbial biomass and interpretingvariations in community structures [13] Ester-linkedmethodwas used for fatty acid methyl ester (FAME) profile analyses[14] The specific procedure to extracting phospholipids wasdivided into six steps (1) 15mL of 02M KOH in methanolwas added to a 35mL centrifuge tube containing 3 g of soil(2)The mixture was incubated at 37∘C for 1 h and during theprocess ester-linked fatty acids were released andmethylatedSamples were vortexed every 10min (3) 3mL of 10M aceticacid and 10mL of hexane were added to the contents inthe tube (4) FAMEs were partitioned into an organic phaseby centrifugation at 4800 r for 10min (5) The hexane layerwas transferred to a clean glass test tube and the hexanewas evaporated under a stream of N

2 (6) FAMEs were

dissolved in 05mL of 1 1 hexane methyl tert-butyl etherand transferred to a GC vial for analysis FAMEs extractedwere detected using a gas chromatograph-mass spectrometer(7890A GC5975C MSD Agilent Technologies Co USA)fitted with an HP-5MS quartz capillary chromatographiccolumn (025mm times 30m times 025 120583m) with an injectortemperature at 250∘C Internal standard for quantificationwas C190 (Sigma-Aldrich Co USA) and external standardfor qualification was GLC NESTLE 37 mix (Nu-Chek)

Bardgett et al [15] previously demonstrated that thecontent and composition of PLFA in the soil reflected thebiomass and structure of soil microbial communities Resultswere analyzed by the MIDI system (Microbial ID Inc)Standard nomenclature was employed to describe FAMEsWe used the PLFA nomenclature pioneered by Frostegard etal [12] and the total content of PLFA to indicate the totalmicrobial biomass Twelve fatty acids (150 i150 a150 i1601611205967 1611205969 170 i170 a170 1811205967 i190 and cy190) werechosen as indicators of bacterial PLFA [16] Fungal PLFA

was represented by 1821205966 [12] anaerobic bacterial PLFAwas represented by cy170 and cy190 [17] aerobic bacterialPLFA was represented by 1611205967 1611205967t and 1811205967 Gram-negative bacterial PLFA and monounsaturated fatty acidswere represented by cy170 and cy190 [18] Gram-positivebacterial PLFAs were represented by five fatty acids (i150a150 i160 i170 and a170) [19]

25 Statistical Analyses Statistical analyses were conductedwith SPSS 170 software for Windows One-way analysis ofvariance (ANOVA) was used to test for significant differencesamong the four successional stages and among the three soillayers in each stage We subdivided the data into three setsvegetation data (average height coverage and biomass) soildata (SOC TN CN ratio pH soil moisture content bulkdensity and salinity) andmicrobial community diversityWeused Duncanrsquos multiple range tests and defined significanceas 119875 lt 005 in both the vertical and horizontal gradientsWe used Spearmanrsquos rank correlations to examine the asso-ciation between the microbial PLFA content and the physic-ochemical characteristics in soil (119875 lt 001) Redundancydiscriminate analysis (RDA) a linear canonical communityordination method was used to explore the vital soil factorsleading to changes in themicrobial community structurewithCanoco for Windows 45 The Monte Carlo permutation test(number of permutations 999) was conducted with 119875 valuesto assess the significance of soil variables in accounting forthe shifts in microbial community parameters

3 Results

31 Soil Physicochemical Analyses Percentage of SOCdecreased vertically but increased along four stages (Table 2)The maximum value of SOC in S1 of stage IV was 18ndash3times that of the other stages and stage I had the lowestvalue Variation in TN followed the same pattern as SOCAlthough CN ratio declined with depth it increased alongsuccession Soil pH ranged from 838 to 931 and increasedwith soil depth Soil salinity values decreased markedly withdeeper soil layers especially in stage I and also decreasedalong with succession stages Moisture content reduced notonly in vertical direction but also along succession Value ofbulk density was the lowest in S1 and decreased with eachsuccessional stage but fluctuated in S2 and S3

32 PLFA Composition and Content We detected 43 PLFAswith the least in stage I (19) increasing in stages II and III(25 and 26 resp) and reached the maximum in stage IV (39)


Table 2 Soil parameters in successional stages

Stage Layer SOC () TN () CN ratio pH Moisture content(g gminus1)

Bulk density(g cmminus3) Salinity ()

IS1 133 (006)Aa 006 (000)Aa 2210 (066)Aa 838 (005)Ae 1878 (043)Aa 131 (006)Aa 522 (018)Aa

S2 129 (002)ABa 003 (001)Ba 2936 (252)Ba 859 (003)Be 2069 (035)Ba 147 (009)Aa 185 (045)Ba

S3 122 (004)Ba 003 (000)Ba 4001 (305)Ca 871 (002)Cf 2170 (035)Ca 147 (006)Aa 094 (069)Ba

IIS1 170 (013)Aab 008 (002)Aa 2005 (162)Aa 890 (001)Aa 1647 (059)Ab 123 (008)Aa 071 (016)Ac

S2 129 (003)Ba 004 (000)Ba 2726 (053)Bb 897 (003)Bb 2073 (036)Ba 140 (005)Ba 084 (003)Bb

S3 123 (001)Ba 003 (001)Bab 3454 (051)Ca 906 (002)Cb 2113 (023)Ba 130 (002)ABabc 078 (002)Ba

IIIS1 229 (039)Ab 014 (004)Aa 1608 (125)Ab 845 (002)Ad 1550 (058)Ab 103 (012)Ab 067 (024)Ac

S2 133 (001)Ba 004 (000)Ba 3543 (126)Bb 874 (002)Ba 1622 (009)Ac 141 (008)Ba 048 (001)Abc

S3 124 (001)Ba 004 (000)Bbc 4316 (258)Cb 877 (001)Ca 1743 (041)Bb 138 (010)Bab 045 (000)Aa

IVS1 412 (088)Ac 033 (008)Ab 1272 (031)Ac 846 (001)Ad 1458 (014)Aa 088 (008)Ac 037 (003)Ac

S2 146 (002)Bb 005 (001)Bb 2761 (331)Bb 904 (006)Bd 1593 (004)Bb 118 (009)Bc 029 (001)Bc

S3 145 (009)Bb 004 (001)Bc 3189 (188)Cb 931 (001)Ce 1708 (042)Cb 117 (015)Bc 022 (001)Ca

Numbers in parentheses are standard errors Capital and small letters represent significant differences among soil depths within the same successional stageand among successional stages within the same soil depth respectively (119875 lt 005)

Table 3 Spearmanrsquos rank correlation analysis between soil microbial PLFA content and soil parameters

Microbialcommunity SOC TN CN ratio Moisture content Bulk density Soil pH Salinity

Total PLFA 0724lowastlowast 0766lowastlowast minus0731lowastlowast minus0799lowastlowast minus0674lowastlowast minus0461lowastlowast nsBacterial PLFA 0753lowastlowast 0760lowastlowast minus0737lowastlowast minus0844lowastlowast minus0777lowastlowast minus0481lowastlowast minus0353lowast

Fungal PLFA 0720lowastlowast 0625lowastlowast minus0587lowastlowast minus0821lowastlowast minus0716lowastlowast ns minus0389lowastlowast

Gram-positivebacterial PLFA 0612lowastlowast 0733lowastlowast minus0735lowastlowast minus0661lowastlowast minus0593lowastlowast minus0356lowast ns

Gram-negativebacterial PLFA 0809lowastlowast 0824lowastlowast minus0803lowastlowast minus0813lowastlowast minus0781lowastlowast minus0509lowastlowast ns

ldquo+rdquo denotes positive correlation and ldquominusrdquo denotes negative correlation lowastlowastSignificant at 119875 lt 001 lowastSignificant at 119875 lt 005 ldquonsrdquo means not significant

As shown in Figure 2(a) (119875 lt 005) total PLFA increasedsignificantly from stages I to IV while vertically values in S1were significantly higher than S2 and S3 (119875 lt 005) Patternfor bacterial (Figure 2(b)) and fungal PLFA (Figure 2(c)) wassimilar to total PLFA By contrast ratio of fungal PLFA tobacterial PLFA (FB ratio) showed the opposite pattern inS2 and S3 with the value increasing as layers are deepening(Figure 2(d))

33 CorrelationAnalysis of PLFAContent and Soil ParametersThe results showed that all types of microbial communitieswere positively correlated with SOC and TN but negativelycorrelated with CN ratio soil moisture content and bulkdensity (Table 3) Although fungi showed no significantcorrelations with pH value PLFA content of all othermicrobes displayed negative correlations with pH valueSalinity showed negative correlations only with bacteria andfungi communities but showed no significant correlationswith other kinds of microbial PLFA content

34 Microbial Community Ratio Alterations Along with ver-tical soil layers deepening the proportion of fungal(Figure 3(a)) andGram-negativebacterial PLFA (Figure 3(b))decreased whereas bacterial and Gram-positive bacterial

PLFA increased In addition there was a large variationbetween S1 and S2 (Figures 3(a) and 3(b)) but a smallvariation between S2 and S3 In successional gradientthe proportion of fungal (Figure 3(a)) and Gram-negativebacterial PLFA (Figure 3(b)) in all layers increased with eachstage whereas bacterial and Gram-positive bacterial PLFAdecreased in all layers

35 RDA Analyses RDA revealed the relationship betweentwo ratios (FB andGram-negative bacteria to Gram-positivebacteria) and seven (SOC TN CN ratio pH moisturecontent bulk density and salinity) key environmental factorsFrom Figure 4 we found that both SOC and TN markedlyaffected FB and Gram-negativeGram-positive ratios (119875 lt0001) while moisture content pH and CN ratio werenegatively correlated with the two ratios and the effect forpH was less than moisture content and CN ratio Besidessalinity and bulk density showed no significant effects on andwere not main environmental factors to the two ratios

4 Discussion

Microbial biomass reflects the size of populations involvedin regulating energy and nutrient cycle of soil [20 21]


Aa

Ab

Ac

Ad

ABa BbBc

Bc

Ba Cab CbCb

0

5

10

15

20

I II III IV

PLFA

cont

ent (

nmol

gminus1)

(a) Total PLFA

Aa

Ab

Ac

Ad

Ba Bb

BcBd

Ba Bb Cb

Bc

0

25

5

75

10

I II III IV

PLFA

cont

ent (

nmol

gminus1)

(b) Bacterial PLFA

S1S2S3

Aa

Aab

Aab

Ab

Ba BbcBc

Bd

BaBb Bb

Bc

0

08

16

24

32

I II III IV

PLFA

cont

ent (

nmol

gminus1)

(c) Fungal PLFA

S1S2S3

AaAa

Aa

Aa

Aa

AaBa

Ab

Aa

Aab Bb

Ac

0

009

018

027

036

FB

ratio

I II III IV

(d) FB ratio

Figure 2 Total PLFA (a) bacterial PLFA (b) fungal PLFA (c) and FB ratio (d) in three layers (S1 S2 and S3) from four successional stages(I) saline-alkali bare land (II) Suaeda glauca (III) Suaeda glauca + Phragmites australis and (IV) Phragmites australis Capital and smallletters represent significant differences among soil depths within the same successional stage and among successional stages within the samesoil depth respectively (119875 lt 005)

Results above suggested that the average height coverageand biomass of dominant species nearly increased alongwith successional stages and also for altitude (Table 1) Inaddition soil parameters (Table 2) affectedmicrobial biomassand structures (Figure 2) Spearmanrsquos correlation analysis(Table 3) showed that all microbial biomass was positivelycorrelated with SOC and TN (119875 lt 001) which suggestedthat SOC and TN levels can be represented by total PLFAbacteria or fungi content Some researchers [22ndash25] havealso reached the same conclusion in other ecosystems Allmicrobe biomass was negatively correlated with CN ratiosoil moisture and bulk density indicating that appropriatepermeability and lower soil moisture content were beneficialto microbes [26] Cook and Papendick [27] reported thatbacteria were active at high water potential levels but fungiat low levels However we found the same results to bacteria(Figure 2(b)) and the opposite result to fungi (Figure 2(c))which may be due to microtopography (Table 1) It is

generally recognized that fungi are more tolerant to droughtthen the reason why the highest value of fungi PLFA contentappeared in successional stage IV is that the plot was locatedat the highest altitude The highest topography gave rise tothe lowest water potential and the most nutritious soil rich inSOC and TN The pH was related to all microbial biomassexcept for fungi in our study However Baath and Anderson[28] reported that microbial biomass especially fungi wasnegatively related with pH Aciego Pietri and Brookes [29]andWu et al [30] reported that soil with higher pHwas richerin Gram-negative than Gram-positive bacteria In our studytotal microbial bacterial and fungal biomass increased alongwith succession accompanying salinity decline It indicatedthat higher salinity inhibited growth of microbes which maybe responsible for sparse vegetation in degraded wetlands[31] Thus soil structure air and water permeability andnutrient influenced microbial communities during vegeta-tion succession [32] and then these factors affected vegetation


0

()

25

50

75

100

S1 S2 S3 S1 S2 S3 S1 S2 S3 S1 S2 S3

Fungal PLFABacterial PLFA

I II III IV

(a)

0

()

25

50

75

100

S1 S2 S3 S1 S2 S3 S1 S2 S3 S1 S2 S3

Gram-negative bacterial PLFAGram-positive bacterial PLFA

I II III IV

(b)

Figure 3 Ratios of fungal to bacterial PLFA (a) and Gram-negative bacterial to Gram-positive bacterial PLFA (b) in three layers (S1 S2 andS3) from four successional stages (I) saline-alkali bare land (II) Suaeda glauca (III) Suaeda glauca+ Phragmites australis and (IV) Phragmitesaustralis

15

SOCFBTN

Gram-negativeGram-positive

pH

SalinityCN ratio

Moisture content

minus10

Bulk density

minus08

10

Figure 4 Redundancy discriminate analysis representing sevenparameters (soil organic carbon total nitrogen CN ratio soilmoisture bulk density pH and salinity) and ratios for twomicrobialgroups fungal PLFAbacterial PLFA and Gram-negativeGram-positive bacteria

development and succession No consensus has been reachedregarding the impact of vegetation on microbes in coastalecosystems Su et al [33] reported that presence or absence ofTypha angustifolia did not influence biomass of bacteria andfungi in sediments of wetlands

Microbial biomass showed obviously vertical distributionand decreased with depth increase (Figure 2) Microbes livedmainly in topsoil which demonstrated that rhizospherewas active interface for mass exchange between soil andplants Total microbial biomass (Figure 2(a)) increased alongsuccession suggesting that succession promoted quantityof microbial accumulation Similar results were observedfor bacteria (Figure 2(b)) and fungi (Figure 2(c)) FB ratio(Figure 2(d)) peaked in S1 of stage IV suggesting that thehigher the FB ratio the greater the stability of wetland

ecosystem and itmeant that Phragmites australis had reachedthe climatic successional stage Therefore FB ratio reflecteddegree of succession de Vries et al [34] reached the sameconclusion Bacteria were dominant in extreme saline-alkaliwetland because it showed higher biomass than fungi ineach successional stage which is consistent with the reportby Li et al [35] In general the greater the amount offungi the better the relative soil condition Fungal biomassrose significantly in stages III and IV as a result of rootsdevelopment by Phragmites australis which reduced soil bulkdensity improved permeability of topsoil and benefited thesurvival of fungi

The proportions of fungi and Gram-negative bacteriaincreased when high carbon material was introduced intothe soil while the proportion of Gram-positive bacteria wasreduced (Figure 3) It could hold true in study by Griffithset al [36] Gram-negative bacteria were dominant microbialgroup The proportion of Gram-negative bacteria increasedalong with vegetation succession By contrast decrease ofGram-positive bacteriamay be due to a uniquemechanism ofadapting acidic environments [37] or pHmay have increasedthe effectiveness of sugars and amino acids to promoteGram-negative bacterial growth RDA also indicated that (Figure 3)the major factors especially SOC and TN impacted on ratiosof microbes (119875 lt 0001)

5 Conclusions

Taken together our study indicated that the evolution of soilmicrobial communities underground in extreme saline-alkaliwetland was closely associated with the succession of vegeta-tion aboveground Microbe biomass and structure changedsignificantly not only along with vegetation succession butalso in vertical soil layersThe colonization of pioneer Suaedaglauca improved the soil condition including the increaseof SOM and TN as well as the decrease of soil density and


salinity It was not due to a single factor but the result ofmultiple cooperating factors SOC and especially TN levelswere themain factors affectingmicrobial communities How-ever soil salinity had no effect on fungibacteria and Gram-negativeGram-positive ratios Microorganism responded tomicroenvironment changes through rhizosphere Bacteriawere dominant and fungi played an important role in soilnutrient cycling with succession

Conflict of Interests

The authors declare that there is no conflict of interestsregarding the publication of this paper

Acknowledgments

This work was supported by the National Science Foundationfor Fostering Talents in Basic Research of National NaturalScience Foundation of China under Grant no J1103503 Tian-jin Wild Plant Resources Survey of Wildlife Conservationand Management Station under Grant 2011FY110300 andFoundation of the Research Center for Eco-EnvironmentalSciences of the Yellow River Delta in Shandong Provinceunder Grant no 2013KFJJ03

References

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[2] D C White W M Davis J S Nickels J D King and R JBobbie ldquoDetermination of the sedimentary microbial biomassby extractible lipid phosphaterdquo Oecologia vol 40 no 1 pp 51ndash62 1979

[3] C R Vossbrinck D C Coleman and T A Woolley ldquoAbioticand biotic factors in litter decomposition in a semiarid grass-landrdquo Ecology vol 60 no 2 pp 265ndash271 1979

[4] J Cortez andM Bouche ldquoDecomposition ofmediterranean leaflitters by Nicodrilus meridionalis (Lumbricidae) in laboratoryand field experimentsrdquo Soil Biology and Biochemistry vol 33no 15 pp 2023ndash2035 2001

[5] J S Singh A S Raghubanshi R S Singh and S C SrivastavaldquoMicrobial biomass acts as a source of plant nutrients in drytropical forest and savannardquoNature vol 338 no 6215 pp 499ndash500 1989

[6] S Roy and J S Singh ldquoConsequences of habitat heterogeneityfor availability of nutrients in a dry tropical forestrdquo Journal ofEcology vol 82 no 3 pp 503ndash509 1994

[7] T Pennanen R Strommer A Markkola and H Fritze ldquoMicro-bial and plant community structure across a primary successiongradientrdquo Scandinavian Journal of Forest Research vol 16 no 1pp 37ndash43 2001

[8] H Zhu X He K Wang Y Su and J Wu ldquoInteractions of veg-etation succession soil bio-chemical properties and microbialcommunities in a Karst ecosystemrdquo European Journal of SoilBiology vol 51 pp 1ndash7 2012

[9] S Yoshitake M Fujiyoshi K Watanabe T Masuzawa TNakatsubo and H Koizumi ldquoSuccessional changes in the soilmicrobial community along a vegetation development sequence

in a subalpine volcanic desert on Mount Fuji Japanrdquo Plant andSoil vol 364 no 1-2 pp 261ndash272 2013

[10] D Cao F C Shi T Koike Z H Lu and J K Sun ldquoHalophyteplant communities affecting enzyme activity and microbes insaline soils of the Yellow River Delta in Chinardquo CLEANmdashSoilAir Water vol 42 no 10 pp 1433ndash1440 2014

[11] L Zelles ldquoFatty acid patterns of phospholipids and lipopolysac-charides in the characterisation of microbial communities insoil a reviewrdquo Biology and Fertility of Soils vol 29 no 2 pp111ndash129 1999

[12] A Frostegard A Tunlid and E Baath ldquoPhospholipid fatty acidcomposition biomass and activity of microbial communitiesfrom two soil types experimentally exposed to different heavymetalsrdquoApplied and Environmental Microbiology vol 59 no 11pp 3605ndash3617 1993

[13] A M Ibekwe and A C Kennedy ldquoPhospholipid fatty acidprofiles and carbon utilization patterns for analysis of microbialcommunity structure under field and greenhouse conditionsrdquoFEMS Microbiology Ecology vol 26 no 2 pp 151ndash163 1998

[14] M E Schutter and R P Dick ldquoComparison of fatty acidmethyl ester (FAME) methods for characterizing microbialcommunitiesrdquo Soil Science Society of America Journal vol 64no 5 pp 1659ndash1668 2000

[15] R D Bardgett P J Hobbs and A Frostegard ldquoChanges insoil fungal bacterial biomass ratios following reductions in theintensity of management of an upland grasslandrdquo Biology andFertility of Soils vol 22 no 3 pp 261ndash264 1996

[16] A Frostegard and E Baath ldquoThe use of phospholipid fatty acidanalysis to estimate bacterial and fungal biomass in soilrdquoBiologyand Fertility of Soils vol 22 no 1-2 pp 59ndash65 1996

[17] J R Vestal and D C White ldquoLipid analysis in microbialecology quantitative approaches to the study of microbialcommunitiesrdquo Bioscience vol 39 no 8 pp 535ndash541 1989

[18] L Zelles ldquoPhospholipid fatty acid profiles in selected membersof soil microbial communitiesrdquo Chemosphere vol 35 no 1-2pp 275ndash294 1997

[19] A Frostegard A Tunlid and E Baath ldquoMicrobial biomassmeasured as total lipid phosphate in soils of different organiccontentrdquo Journal of Microbiological Methods vol 14 no 3 pp151ndash163 1991

[20] K Arunachalam A Arunachalam and N P Melkania ldquoInflu-ence of soil properties on microbial populations activity andbiomass in humid subtropical mountainous ecosystems ofIndiardquo Biology and Fertility of Soils vol 30 no 3 pp 217ndash2231999

[21] J P Taylor BWilsonM SMills andRG Burns ldquoComparisonof microbial numbers and enzymatic activities in surfacesoils and subsoils using various techniquesrdquo Soil Biology andBiochemistry vol 34 no 3 pp 387ndash401 2002

[22] D S Jenkinson and D S Powlson ldquoThe effects of biocidaltreatments on metabolism in soilmdashV a method for measuringsoil biomassrdquo Soil Biology and Biochemistry vol 8 no 3 pp209ndash213 1976

[23] H Insam and K H Domsch ldquoRelationship between soilorganic carbon and microbial biomass on chronosequences ofreclamation sitesrdquoMicrobial Ecology vol 15 no 2 pp 177ndash1881988

[24] D M Mao Y W Min L L Yu R Martens and H InsamldquoEffect of afforestation onmicrobial biomass and activity in soilsof tropical Chinardquo Soil Biology amp Biochemistry vol 24 no 9 pp865ndash872 1992


[25] H Y Yao Z L He and C Y Huang ldquoPhospholipid fatty acidprofiles of chinese red soils with varying fertility levels and landuse historiesrdquo Pedosphere vol 11 no 2 pp 97ndash103 2001

[26] M A Williams and C W Rice ldquoSeven years of enhancedwater availability influences the physiological structural andfunctional attributes of a soil microbial communityrdquo AppliedSoil Ecology vol 35 no 3 pp 535ndash545 2007

[27] R J Cook and R I Papendick ldquoSoil water potential as a factorin the ecology of Fusarium roseum f sp cerealis lsquoCulmorumrsquordquoPlant and Soil vol 32 no 1 pp 131ndash145 1970

[28] E Baath and T H Anderson ldquoComparison of soil fun-galbacterial ratios in a pH gradient using physiological andPLFA-based techniquesrdquo Soil Biology and Biochemistry vol 35no 7 pp 955ndash963 2003

[29] J C Aciego Pietri and P C Brookes ldquoSubstrate inputs and pH asfactors controlling microbial biomass activity and communitystructure in an arable soilrdquo Soil Biology and Biochemistry vol41 no 7 pp 1396ndash1405 2009

[30] Y Wu B Ma L Zhou et al ldquoChanges in the soil microbialcommunity structure with latitude in eastern China based onphospholipid fatty acid analysisrdquo Applied Soil Ecology vol 43no 2-3 pp 234ndash240 2009

[31] S Tripathi S Kumari A Chakraborty A Gupta KChakrabarti and B K Bandyapadhyay ldquoMicrobial biomassand its activities in salt-affected coastal soilsrdquo Biology andFertility of Soils vol 42 no 3 pp 273ndash277 2006

[32] N Fierer J P Schimel and P A Holden ldquoVariations inmicrobial community composition through two soil depthprofilesrdquo Soil Biology amp Biochemistry vol 35 no 1 pp 167ndash1762003

[33] R Su R N Lohner K A Kuehn R Sinsabaugh and RK Neely ldquoMicrobial dynamics associated with decomposingTypha angustifolia litter in two contrasting Lake Erie coastalwetlandsrdquoAquaticMicrobial Ecology vol 46 no 3 pp 295ndash3072007

[34] F T de Vries E Hoffland N van Eekeren L Brussaard and JBloem ldquoFungalbacterial ratios in grasslands with contrastingnitrogen managementrdquo Soil Biology amp Biochemistry vol 38 no8 pp 2092ndash2103 2006

[35] J-J Li Y-M Zheng J-X Yan H-J Li and J-Z He ldquoSuccessionof plant and soil microbial communities with restoration ofabandoned land in the Loess Plateau Chinardquo Journal of Soilsand Sediments vol 13 no 4 pp 760ndash769 2013

[36] B S Griffiths K Ritz N Ebblewhite and G Dobson ldquoSoilmicrobial community structure effects of substrate loadingratesrdquo Soil Biology amp Biochemistry vol 31 no 1 pp 145ndash1531999

[37] P D Cotter and C Hill ldquoSurviving the acid test responses ofgram-positive bacteria to low pHrdquoMicrobiology and MolecularBiology Reviews vol 67 no 3 pp 429ndash453 2003

Submit your manuscripts athttpwwwhindawicom

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Inorganic ChemistryInternational Journal of

Hindawi Publishing Corporation httpwwwhindawicom Volume 2014

International Journal ofPhotoenergy


Carbohydrate Chemistry

International Journal of


Journal of

Chemistry


Advances in

Physical Chemistry

Hindawi Publishing Corporationhttpwwwhindawicom

Analytical Methods in Chemistry

Journal of

Volume 2014

Bioinorganic Chemistry and ApplicationsHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

SpectroscopyInternational Journal of


The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Medicinal ChemistryInternational Journal of


Chromatography Research International


Applied ChemistryJournal of



Theoretical ChemistryJournal of


Journal of

Spectroscopy

Analytical ChemistryInternational Journal of


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Quantum Chemistry


Organic Chemistry International

ElectrochemistryInternational Journal of



CatalystsJournal of


Tianjin

0 125 25(km)

SS

Bohai Bay

Beidag

ang

SS

Beidagang ReservoirBL

SGSG+PA

PA

Bohai Bay

N

W E

S

117∘09

9984000998400998400E 117

∘21

9984000998400998400E 117

∘33

9984000998400998400E 117

∘45

9984000998400998400E 117

∘57

9984000998400998400E

39∘03

9984000998400998400N

37∘57

9984000998400998400N

38∘51

9984000998400998400N

38∘45

9984000998400998400N

38∘39

9984000998400998400N

Figure 1 Locations of study and sample sites (SS) near the Bohai Bay Details of the plots and abbreviation names of dominant species arelisted in Table 1

The aims of this study were to elucidate (1) the response ofmicroorganism community structural composition to alongwith environmental changes caused by halophyte successionand (2) main factors influencing soil microbial commu-nity structure along with succession The results of thisstudy may offer critical information for ecological restora-tion and soil quality improvement in severe saline-alkaliwetlands

2 Materials and Methods

21 Study Sites It was located in the southeast of Tianjin nearBohai Bay middle-east of China (117∘271015840E 38∘431015840N) (Figure 1and Table 1) It was characterized by a warm semihumidcontinental monsoon climate Annual mean temperaturewas approximately 122∘C with the coldest (January) andhottest (July) mean temperatures of 35∘C and 262∘C respec-tively Annual mean precipitation was 520ndash660mm and 75was summer rainfall (JulyndashSeptember) The study area wascovered by extreme saline-alkali soil together with larger

amount of evaporation and smaller amount of precipitationThe soil in this area was barren Landform was a coastalfloodplain with sparse vegetation

22 Soil Sampling We investigated four community typeswith three repetitions in June 2013 Table 1 summarized theinformation of four successional stages covering averageheight coverage biomass and altitude of dominant speciesThe four typical communities examined were (I) saline-alkalibare land (BL) (II) Suaeda glauca community (SG) (III)Suaeda glauca + Phragmites australis community (SG + PA)and (IV) Phragmites australis community (PA) Soil sampleswere collected using multipoint mixed method with threevertical layers S1 (0ndash10 cm) S2 (10ndash20 cm) and S3 (20ndash30 cm) We collected in two times on account of differentanalyses One set was used to measure bulk density andmoisture content by a cutting ring Another set was dividedinto twoparts for PLFAanalysis kept atminus20∘C for parameteranalyses dried in shade homogenized and sieved beforepreserved








2 (6) FAMEs were





3 Results
































4 Discussion



Aa

Ab

Ac

Ad

ABa BbBc

Bc

Ba Cab CbCb

0

5

10

15

20

I II III IV

PLFA

cont

ent (

nmol

gminus1)

(a) Total PLFA

Aa

Ab

Ac

Ad

Ba Bb

BcBd

Ba Bb Cb

Bc

0

25

5

75

10

I II III IV

PLFA

cont

ent (

nmol

gminus1)

(b) Bacterial PLFA

S1S2S3

Aa

Aab

Aab

Ab

Ba BbcBc

Bd

BaBb Bb

Bc

0

08

16

24

32

I II III IV

PLFA

cont

ent (

nmol

gminus1)

(c) Fungal PLFA

S1S2S3

AaAa

Aa

Aa

Aa

AaBa

Ab

Aa

Aab Bb

Ac

0

009

018

027

036

FB

ratio

I II III IV

(d) FB ratio





0

()

25

50

75

100

S1 S2 S3 S1 S2 S3 S1 S2 S3 S1 S2 S3


I II III IV

(a)

0

()

25

50

75

100

S1 S2 S3 S1 S2 S3 S1 S2 S3 S1 S2 S3


I II III IV

(b)


15

SOCFBTN


pH

SalinityCN ratio

Moisture content

minus10

Bulk density

minus08

10






5 Conclusions






Acknowledgments


References

















































Journal of

Chemistry


Advances in

Physical Chemistry



Journal of

Volume 2014














Journal of

Spectroscopy



Journal of


Quantum Chemistry






CatalystsJournal of








2 (6) FAMEs were





3 Results
































4 Discussion



Aa

Ab

Ac

Ad

ABa BbBc

Bc

Ba Cab CbCb

0

5

10

15

20

I II III IV

PLFA

cont

ent (

nmol

gminus1)

(a) Total PLFA

Aa

Ab

Ac

Ad

Ba Bb

BcBd

Ba Bb Cb

Bc

0

25

5

75

10

I II III IV

PLFA

cont

ent (

nmol

gminus1)

(b) Bacterial PLFA

S1S2S3

Aa

Aab

Aab

Ab

Ba BbcBc

Bd

BaBb Bb

Bc

0

08

16

24

32

I II III IV

PLFA

cont

ent (

nmol

gminus1)

(c) Fungal PLFA

S1S2S3

AaAa

Aa

Aa

Aa

AaBa

Ab

Aa

Aab Bb

Ac

0

009

018

027

036

FB

ratio

I II III IV

(d) FB ratio





0

()

25

50

75

100

S1 S2 S3 S1 S2 S3 S1 S2 S3 S1 S2 S3


I II III IV

(a)

0

()

25

50

75

100

S1 S2 S3 S1 S2 S3 S1 S2 S3 S1 S2 S3


I II III IV

(b)


15

SOCFBTN


pH

SalinityCN ratio

Moisture content

minus10

Bulk density

minus08

10






5 Conclusions






Acknowledgments


References

















































Journal of

Chemistry


Advances in

Physical Chemistry



Journal of

Volume 2014














Journal of

Spectroscopy



Journal of


Quantum Chemistry






CatalystsJournal of






























4 Discussion



Aa

Ab

Ac

Ad

ABa BbBc

Bc

Ba Cab CbCb

0

5

10

15

20

I II III IV

PLFA

cont

ent (

nmol

gminus1)

(a) Total PLFA

Aa

Ab

Ac

Ad

Ba Bb

BcBd

Ba Bb Cb

Bc

0

25

5

75

10

I II III IV

PLFA

cont

ent (

nmol

gminus1)

(b) Bacterial PLFA

S1S2S3

Aa

Aab

Aab

Ab

Ba BbcBc

Bd

BaBb Bb

Bc

0

08

16

24

32

I II III IV

PLFA

cont

ent (

nmol

gminus1)

(c) Fungal PLFA

S1S2S3

AaAa

Aa

Aa

Aa

AaBa

Ab

Aa

Aab Bb

Ac

0

009

018

027

036

FB

ratio

I II III IV

(d) FB ratio





0

()

25

50

75

100

S1 S2 S3 S1 S2 S3 S1 S2 S3 S1 S2 S3


I II III IV

(a)

0

()

25

50

75

100

S1 S2 S3 S1 S2 S3 S1 S2 S3 S1 S2 S3


I II III IV

(b)


15

SOCFBTN


pH

SalinityCN ratio

Moisture content

minus10

Bulk density

minus08

10






5 Conclusions






Acknowledgments


References

















































Journal of

Chemistry


Advances in

Physical Chemistry



Journal of

Volume 2014














Journal of

Spectroscopy



Journal of


Quantum Chemistry






CatalystsJournal of


Aa

Ab

Ac

Ad

ABa BbBc

Bc

Ba Cab CbCb

0

5

10

15

20

I II III IV

PLFA

cont

ent (

nmol

gminus1)

(a) Total PLFA

Aa

Ab

Ac

Ad

Ba Bb

BcBd

Ba Bb Cb

Bc

0

25

5

75

10

I II III IV

PLFA

cont

ent (

nmol

gminus1)

(b) Bacterial PLFA

S1S2S3

Aa

Aab

Aab

Ab

Ba BbcBc

Bd

BaBb Bb

Bc

0

08

16

24

32

I II III IV

PLFA

cont

ent (

nmol

gminus1)

(c) Fungal PLFA

S1S2S3

AaAa

Aa

Aa

Aa

AaBa

Ab

Aa

Aab Bb

Ac

0

009

018

027

036

FB

ratio

I II III IV

(d) FB ratio





0

()

25

50

75

100

S1 S2 S3 S1 S2 S3 S1 S2 S3 S1 S2 S3


I II III IV

(a)

0

()

25

50

75

100

S1 S2 S3 S1 S2 S3 S1 S2 S3 S1 S2 S3


I II III IV

(b)


15

SOCFBTN


pH

SalinityCN ratio

Moisture content

minus10

Bulk density

minus08

10






5 Conclusions






Acknowledgments


References

















































Journal of

Chemistry


Advances in

Physical Chemistry



Journal of

Volume 2014














Journal of

Spectroscopy



Journal of


Quantum Chemistry






CatalystsJournal of


0

()

25

50

75

100

S1 S2 S3 S1 S2 S3 S1 S2 S3 S1 S2 S3


I II III IV

(a)

0

()

25

50

75

100

S1 S2 S3 S1 S2 S3 S1 S2 S3 S1 S2 S3


I II III IV

(b)


15

SOCFBTN


pH

SalinityCN ratio

Moisture content

minus10

Bulk density

minus08

10






5 Conclusions






Acknowledgments


References

















































Journal of

Chemistry


Advances in

Physical Chemistry



Journal of

Volume 2014














Journal of

Spectroscopy



Journal of


Quantum Chemistry






CatalystsJournal of





Acknowledgments


References

















































Journal of

Chemistry


Advances in

Physical Chemistry



Journal of

Volume 2014














Journal of

Spectroscopy



Journal of


Quantum Chemistry






CatalystsJournal of
























Journal of

Chemistry


Advances in

Physical Chemistry



Journal of

Volume 2014














Journal of

Spectroscopy



Journal of


Quantum Chemistry






CatalystsJournal of

research article soil microbial community structure...

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